Genetic Analysis of Arrhythmogenic Diseases in the Era of NGS: The Complexity of Clinical Decision-Making in Brugada Syndrome

PLoS One. 2015 Jul 31;10(7):e0133037. doi: 10.1371/journal.pone.0133037. eCollection 2015.

Abstract

Background: The use of next-generation sequencing enables a rapid analysis of many genes associated with sudden cardiac death in diseases like Brugada Syndrome. Genetic variation is identified and associated with 30-35% of cases of Brugada Syndrome, with nearly 20-25% attributable to variants in SCN5A, meaning many cases remain undiagnosed genetically. To evaluate the role of genetic variants in arrhythmogenic diseases and the utility of next-generation sequencing, we applied this technology to resequence 28 main genes associated with arrhythmogenic disorders.

Materials and methods: A cohort of 45 clinically diagnosed Brugada Syndrome patients classified as SCN5A-negative was analyzed using next generation sequencing. Twenty-eight genes were resequenced: AKAP9, ANK2, CACNA1C, CACNB2, CASQ2, CAV3, DSC2, DSG2, DSP, GPD1L, HCN4, JUP, KCNE1, KCNE2, KCNE3, KCNH2, KCNJ2, KCNJ5, KCNQ1, NOS1AP, PKP2, RYR2, SCN1B, SCN3B, SCN4B, SCN5A, SNTA1, and TMEM43. A total of 85 clinically evaluated relatives were also genetically analyzed to ascertain familial segregation.

Results and discussion: Twenty-two patients carried 30 rare genetic variants in 12 genes, only 4 of which were previously associated with Brugada Syndrome. Neither insertion/deletion nor copy number variation were detected. We identified genetic variants in novel candidate genes potentially associated to Brugada Syndrome. These include: 4 genetic variations in AKAP9 including a de novo genetic variation in 3 positive cases; 5 genetic variations in ANK2 detected in 4 cases; variations in KCNJ2 together with CASQ2 in 1 case; genetic variations in RYR2, including a de novo genetic variation and desmosomal proteins encoding genes including DSG2, DSP and JUP, detected in 3 of the cases. Larger gene panels or whole exome sequencing should be considered to identify novel genes associated to Brugada Syndrome. However, application of approaches such as whole exome sequencing would difficult the interpretation for clinical purposes due to the large amount of data generated. The identification of these genetic variants opens new perspectives on the implications of genetic background in the arrhythmogenic substrate for research purposes.

Conclusions: As a paradigm for other arrhythmogenic diseases and for unexplained sudden death, our data show that clinical genetic diagnosis is justified in a family perspective for confirmation of genetic causality. In the era of personalized medicine using high-throughput tools, clinical decision-making is increasingly complex.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • A Kinase Anchor Proteins / genetics
  • Adult
  • Ankyrins / genetics
  • Arrhythmias, Cardiac / genetics
  • Brugada Syndrome / diagnosis*
  • Brugada Syndrome / genetics*
  • Calsequestrin / genetics
  • Clinical Decision-Making
  • Cohort Studies
  • Cytoskeletal Proteins / genetics
  • Death, Sudden, Cardiac
  • Desmoglein 2 / genetics
  • Desmoplakins / genetics
  • Female
  • Genetic Testing
  • Genetic Variation*
  • High-Throughput Nucleotide Sequencing
  • Humans
  • Male
  • Middle Aged
  • NAV1.5 Voltage-Gated Sodium Channel / genetics
  • Pedigree
  • Penetrance
  • Potassium Channels, Inwardly Rectifying / genetics
  • Retrospective Studies
  • Ryanodine Receptor Calcium Release Channel / genetics
  • Sequence Analysis, DNA
  • gamma Catenin

Substances

  • A Kinase Anchor Proteins
  • AKAP9 protein, human
  • ANK2 protein, human
  • Ankyrins
  • CASQ2 protein, human
  • Calsequestrin
  • Cytoskeletal Proteins
  • DSG2 protein, human
  • DSP protein, human
  • Desmoglein 2
  • Desmoplakins
  • JUP protein, human
  • KCNJ2 protein, human
  • NAV1.5 Voltage-Gated Sodium Channel
  • Potassium Channels, Inwardly Rectifying
  • Ryanodine Receptor Calcium Release Channel
  • SCN5A protein, human
  • gamma Catenin

Grants and funding

This work was supported by CA: Instituto de Salud Carlos III (FIS-PI11/01826); RB: Fundació La Caixa; and RB: Centro Nacional de Investigaciones Cardiovasculares (CNIC-03-2008).